Full-likelihood genomic analysis clarifies a complex history of species divergence and introgression: the example of the erato-sara group of Heliconius butterflies

Introgressive hybridization plays a key role in adaptive evolution and
species diversification in many groups of species. However,
frequent hybridization and gene flow between species make estimation of
the species phylogeny and key population parameters
challenging. Here, we show that by accounting for phasing and
using full-likelihood methods, introgression histories and population
parameters can be estimated reliably from whole-genome sequence
data. We employ the multispecies coalescent (MSC) model with and
without gene flow to infer the species phylogeny and cross-species
introgression events using genomic data from six members of the erato-sara
clade of Heliconius butterflies. The methods naturally accommodate random
fluctuations in genealogical history across the genome due to deep
coalescence. To avoid heterozygote phasing errors in haploid sequences
commonly produced by genome assembly methods, we process and compile
unphased diploid sequence alignments and use analytical methods to average
over uncertainties in heterozygote phase resolution. There is
robust evidence for introgression across the genome, both among distantly
related species deep in the phylogeny and between sister species in
shallow parts of the tree. We obtain chromosome-specific
estimates of key population parameters such as introgression directions,
times and probabilities, as well as species divergence times and
population sizes for modern and ancestral species. We confirm
ancestral gene flow between the sara clade and an ancestral population of
H. telesiphe, a likely hybrid speciation origin for H. hecalesia, and gene
flow between the sister species H. erato and H. himera. Inferred
introgression among ancestral species also explains the history of two
chromosomal inversions deep in the phylogeny of the group. This study
illustrates how a full-likelihood approach based on the multispecies
coalescent makes it possible to extract rich historical information of
species divergence and gene flow from genomic data.